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Sectorial mutagenesis by transposable elements

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Abstract

Transposable elements (TEs) generate insertions and cause other mutations in the genomic DNA. It is proposed that during co-evolution between TEs and eukaryotic genomes, an optimal path of the insertion mutagenesis is determined by the surviving TEs. These TEs can become semi-permanently established, chromatin-regulated ‘source’ or ‘mutator genes’, responsible for targeting insertion mutations to specific chromosomal regions. Such mutations can manifest themselves in non-random distribution patterns of interspersed repeats in eukaryotic chromosomes. In this paper we discuss specific models, examples and implications of optimized mutagenesis in eukaryotes.

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References

  • Agrawal, A., Q.M. Eastman & D.G. Schatz, 1998. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394: 744–751.

    Article  PubMed  CAS  Google Scholar 

  • Bernardi, G., 1989. The isochore organization of the human genome. Annu. Rev. Genet. 23: 637–661.

    Article  PubMed  CAS  Google Scholar 

  • Bernardi, G., 1995. The human genome: organization and evolutionary history. Annu. Rev. Genet. 29: 445–476.

    Article  PubMed  CAS  Google Scholar 

  • Bird, A., 1997. Does DNA methylation control transposition of selfish elements in germline? Trends Genet. 13: 469–470.

    Article  PubMed  CAS  Google Scholar 

  • Boyle, A.L., S.G. Ballard & D.C. Ward, 1990. Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization. Proc. Natl. Acad. Sci. USA 87: 7757–7761.

    Article  PubMed  CAS  Google Scholar 

  • Britten, R.J., W.F. Baron, D.B. Stout & E.H. Davidson, 1988, Sources and evolution of human Alu repeated sequences. Proc. Natl. Acad. Sci. USA 85: 4770–4774.

    Article  PubMed  CAS  Google Scholar 

  • Chen, T.L. & L. Manuelidis, 1989. SINEs and LINEs cluster in distinct DNA fragments of Giemsa band size. Chromosoma 98: 309–316.

    Article  PubMed  CAS  Google Scholar 

  • Cherry, S.R. & D. Baltimore, 1999. Chromatin remodeling directly activates V(D)J recombination. Proc. Natl. Acad. Sci. USA 96: 10788–10793.

    Article  PubMed  CAS  Google Scholar 

  • Craig, J.M. & W.A. Bickmore, 1997. The relationship between gene density and chromosome banding patterns in mammalian nuclei, pp. 65–83 in Chromosomes Today, edited by N. Henriques-Gil, J. S. Parker and M. J. Puertas. Chapman & Hall, London, UK.

    Google Scholar 

  • de Souza, S.J., M. Long, R.J. Klein, S. Roy, S. Lin et al., 1998. Toward a resolution of the introns early/late debate: only phase zero introns are correlated with the structure of ancient proteins. Proc. Natl. Acad. Sci. USA 95: 5094–5099.

    Article  PubMed  CAS  Google Scholar 

  • Deininger, P.L. & M.A. Batzer, 1999 Alu repeats and human disease. Mol. Genet. Metab. 67: 183–193.

    Article  PubMed  CAS  Google Scholar 

  • Dhellin, O., J. Maestre & T. Heidmann, 1997. Functional differences between the human LINE retrotransposon and retroviral reverse transcriptases for in vivo reverse transcription. EMBO J. 16: 6590–6602.

    Article  PubMed  CAS  Google Scholar 

  • Dimitri, P., 1997. Constitutive heterochromatin and transposable elements in Drosophila melanogaster. Genetica 100: 85–93.

    Article  PubMed  CAS  Google Scholar 

  • Donovan, G.P., C. Harden, J. Gal, L. Ho, E. Sibille et al., 1997. Sensitivity to jerky gene dosage underlies epileptic seizures in mice. J. Neurosci. 17: 4562–4569.

    PubMed  CAS  Google Scholar 

  • Doolittle, W.F. & C. Sapienza, 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–603.

    Article  PubMed  CAS  Google Scholar 

  • Duret, L., D. Mouchiroud & C. Gautier, 1995. Statistical analysis of vertebrate sequences reveals that long genes are scarce in GC-rich isochores. J. Mol. Evol. 40: 308–317.

    Article  PubMed  CAS  Google Scholar 

  • Halverson, D., M. Baum, J. Stryker, J. Carbon & L. Clarke, 1997. A centromere DNA-binding protein from fission yeast affects chromosome segregation and has homology to human CENP-B. J. Cell Biol. 136: 487–500.

    Article  PubMed  CAS  Google Scholar 

  • Hartl, D.L., E.R. Lozovskaya, D.I. Nurminsky & A.R. Lohe, 1997. What restricts the activity of mariner-like transposable elements? Trends Genet. 13: 197–201.

    Article  PubMed  CAS  Google Scholar 

  • Hiom, K., M. Melek & M. Gellert, 1998. DNA transposition by the RAG1 and RAG2 proteins: A possible source of oncogenic translocations. Cell 94: 463–470.

    Article  PubMed  CAS  Google Scholar 

  • Holmquist, G.P., 1992. Chromosome bands, their chromatin flavors, and their functional features. Am. J. Hum. Genet. 51: 17–37.

    PubMed  CAS  Google Scholar 

  • Hu, X. & R.G. Worton, 1992. Partial gene duplication as a cause of human disease. Hum. Mutat. 1: 3–12.

    Article  PubMed  CAS  Google Scholar 

  • Jabbari, K. & G. Bernardi, 1998. CpG doublets, CpG islands and Alu repeats in long human DNA sequences from different isochore families. Gene 224: 123–128.

    Article  PubMed  CAS  Google Scholar 

  • Jackson, D.A., 1997. Chromatin domains and nuclear compartments: establishing sites of gene expression in eukaryotic nuclei. Mol. Biol. Rep. 24: 209–220.

    Article  PubMed  CAS  Google Scholar 

  • Jensen, S., M.P. Gassama & T. Heidmann, 1999. Taming of transposable elements by homology-dependent gene silencing. Nat. Genet. 21: 209–212.

    Article  PubMed  CAS  Google Scholar 

  • Jurka, J., 1989. Subfamily structure and evolution of the human L1 family of repetitive sequences. J. Mol. Evol. 29: 496–503.

    PubMed  CAS  Google Scholar 

  • Jurka, J., 1995. Origin and evolution of Alu repetitive elements, pp. 25–41 in The Impact of Short Interspersed Elements (SINEs) on the Host genome, edited by R.J. Maraia. R.G. Landes Company, Austin.

    Google Scholar 

  • Jurka, J., 1997 Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc. Natl. Acad. Sci. USA 94: 1872–1877.

    Article  PubMed  CAS  Google Scholar 

  • Jurka, J., 1998. Repeats in genomic DNA: mining and meaning. Curr. Opin. Struct. Biol. 8: 333–337.

    Article  PubMed  CAS  Google Scholar 

  • Jurka, J. & A. Milosavljevic, 1991, Reconstruction and analysis of human Alu genes. J. Mol. Evol. 32: 105–121.

    PubMed  CAS  Google Scholar 

  • Jurka, J. & T. Smith, 1988. A fundamental division in the Alu family of repeated sequences. Proc. Natl. Acad. Sci. USA 85: 4775–4778.

    Article  PubMed  CAS  Google Scholar 

  • Jurka, J., E. Zietkiewicz & D. Labuda, 1995. Ubiquitous mammalian interspersed repeats (MIRs) are molecular fossils from the Mesozoic era. Nucl. Acids Res. 23: 170–175.

    PubMed  CAS  Google Scholar 

  • Jurka, J., V.V. Kapitonov, P. Klonowski, J. Walichiewicz & A.F.A. Smit, 1996. Identification of new medium reiteration frequency repeats in the genomes of primates, rodentia and lagomorpha. Genetica 98: 235–247.

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov, V.V. & J. Jurka, 1996 The age of Alu subfamilies. J. Mol. Evol. 42: 59–65.

    Article  PubMed  CAS  Google Scholar 

  • Kapitonov, V. & J. Jurka, 1998. MER53, a non-autonomous DNA transposon associated with a variety of functionally related defense genes in the human genome. DNA Sequence 8: 277–288.

    Article  PubMed  CAS  Google Scholar 

  • Kaplan, N., T. Darden & C.H. Langley, 1985. Evolution and extinction of transposable elements in Mendelian populations. Genetics 109: 459–480.

    PubMed  CAS  Google Scholar 

  • Kazazian, H.H. Jr. & J.V. Moran, 1998. The impact of L1 retrotransposons on the human genome. Nat. Genet. 19: 19–24.

    PubMed  CAS  Google Scholar 

  • Kidwell, M.G. & D. Lisch, 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94: 7704–7711.

    Article  PubMed  CAS  Google Scholar 

  • Kipling, D. & P.E. Warburton, 1997. Centromeres, CENP-B and Tigger too. Trends Genet. 13: 141–145.

    Article  PubMed  CAS  Google Scholar 

  • Korenberg, J.R. & M.C. Rykowski, 1988. Human genome organization: Alu, Lines and the molecular structure of metaphase chromosome bands. Cell 53: 391–400.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, S., K. Tamamura & M. Nei, 1994. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput. Appl. Biosci. 10: 189–191.

    PubMed  CAS  Google Scholar 

  • Labrador, M. & V.G. Corces, 1997. Transposable element-host interactions: regulation of insertion and excision. Ann. Rev. Biochem. 31: 381–404.

    CAS  Google Scholar 

  • Lewis, S.M., 1999. Evolution of immunoglobulin and T-cell receptor gene assembly. Ann. N Y Acad. Sci. 870: 58–67.

    Article  PubMed  CAS  Google Scholar 

  • Ligner, J., T.R. Hughes, A. Shevchenko, M. Mann, V. Lundblad et al., 1997. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561–567.

    Article  Google Scholar 

  • Logsdon, J.M., Jr. & J.D. Palmer, 1994. Origin of introns — early or late? Nature 369: 526.

    Article  PubMed  Google Scholar 

  • Malick, H.S., W.D. Burke & T.H. Eickbush, 1999. The age and evolution of non-LTR retrotranposable elements. Mol. Biol. Evol. 16: 793–805.

    Google Scholar 

  • Manuelidis, L. & D.C. Ward, 1984. Chromosomal and nuclear distribution of the 1.9-kb human DNA repeat segment. Chromosoma 91: 28–38.

    Article  PubMed  CAS  Google Scholar 

  • Matassi, G., D. Labuda & G. Bernardi, 1998. Distribution of mammalian-wide interspersed repeats (MIRs) in the isochores of the human genome. FEBS Lett. 439: 63–65.

    Article  PubMed  CAS  Google Scholar 

  • Matzke, M.A. & A.J. Matzke, 1998. Epigenetic silencing of plant transgenes as a consequence of diverse cellular defence responses. Cell. Mol. Life Sci. 54: 94–103.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J.F., 1993. Evolution and consequences of transposable elements. Curr. Opin. Genet. Dev. 3: 855–864.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J.F., 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10: 123–126.

    Article  Google Scholar 

  • Miki, Y., 1998. Retrotransposal integration of mobile genetic elements in human diseases. J. Hum. Genet. 43: 77–84.

    Article  PubMed  CAS  Google Scholar 

  • Nakamura, T.M., B.M. Gregg, K.B. Chapman, S.L. Weinrich, W.H. Andrews et al., 1997. Telomerase catalytic subunit homologs from fission yeast and human. Science 277: 955–959.

    Article  PubMed  CAS  Google Scholar 

  • Okada, N., M. Hamada, I. Ogiwara & K. Ohshima, 1997. SINEs and LINEs share common 3′ sequences: a review. Gene 205: 229–243.

    Article  PubMed  CAS  Google Scholar 

  • Orgel, L.E. & F.H.C. Crick, 1980. Selfish DNA: the ultimate parasite. Nature 284: 604–607.

    Article  PubMed  CAS  Google Scholar 

  • Pardue, M.L., O.N. Danilevskaya, K.L. Traverse & K. Lowenhaupt, 1997. Evolutionary links between telomeres and transposable elements. Genetica 100: 73–84.

    Article  PubMed  CAS  Google Scholar 

  • Pirrotta, V. & L. Rastelli, 1994. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. Bioessays 16: 549–556.

    Article  PubMed  CAS  Google Scholar 

  • Robertson, H.M., 1996. Members of pogo superfamily of DNA-mediated transposons in the human genome. Mol. Gen. Genet. 252: 761–766.

    Article  PubMed  CAS  Google Scholar 

  • Roger, A.J., P.J. Keeling & W.F. Doolittle, 1994. Introns, the broken transposons. Soc. Gen. Physiol. Ser. 49: 27–37.

    PubMed  CAS  Google Scholar 

  • Roth, D.B. & N.L. Craig, 1998. VDJ Recombination: A transposase goes to work. Cell 94: 411–414.

    Article  PubMed  CAS  Google Scholar 

  • Schmid, C.W., 1998. Does SINE evolution preclude Alu function? Nucl. Acids Res. 26: 4541–4550.

    Article  PubMed  CAS  Google Scholar 

  • Shapiro, J.A., 1999. Genome system architecture and natural genetic engineering in evolution. Ann. N. Y. Acad. Sci. 870: 23–35.

    Article  PubMed  CAS  Google Scholar 

  • Smit, A.F.A., 1996. The origin of interspersed repeats in the human genome. Curr. Opin. Genet. Dev. 6: 743–748.

    Article  PubMed  CAS  Google Scholar 

  • Smit, A.F.A. & A.D. Riggs, 1996. Tiggers and other DNA transposon fossils in the human genome. Proc. Natl. Acad. Sci. USA 93: 1443–1448.

    Article  PubMed  CAS  Google Scholar 

  • Smit, A.F.A., G. Toth, A.D. Riggs & J. Jurka, 1995. Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences. J. Mol. Biol. 246: 401–417.

    Article  PubMed  CAS  Google Scholar 

  • Soriano, P., M. Meunier-Rotival & G. Bernardi, 1983. The distribution of interspersed repeats is nonuniform and conserved in the mouse and human genomes. Proc. Natl. Acad. Sci. USA 80: 1816–1820.

    Article  PubMed  CAS  Google Scholar 

  • Stoltzfus, A., D.F. Spencer, M. Zuker, J.M. Logsdon, Jr. & W.F. Doolittle, 1994. Testing the exon theory of genes:the evidence from protein structure. Science 265: 202–207.

    PubMed  CAS  Google Scholar 

  • Surzycki, S.A. & W.R. Belknap, 2000. Repetitive-DNA elements are similarly distributed on Caenorhabditis elegans chromosomes. Proc. Natl. Acad. Sci. USA 97: 245–249.

    Article  PubMed  CAS  Google Scholar 

  • Szmulewicz, M.N., G.E. Novick & R.J. Herrera, 1998. Effects of Alu insertions on gene function. Electrophoresis 19: 1260–1264.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J.D., D.G. Higgins & T.J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.

    PubMed  CAS  Google Scholar 

  • Toth, M., J. Grimsby, G. Buzsaki & G.P. Donovan, 1995. Epileptic seizures caused by inactivation of a novel gene, jerky, related to centromere binding protein-B in transgenic mice. Nat. Genet. 11: 71–75.

    Article  PubMed  CAS  Google Scholar 

  • von Sternberg, R.M., G.E. Novick, G.-P. Gao & R.J. Herrera, 1992. Genome canalization: the coevolution of transposable and interspersed repetitive elements with single copy DNA. Genetica 86: 215–246.

    Article  PubMed  CAS  Google Scholar 

  • von Sternberg, R., 1996. The role of constrained self-organization in genome structural evolution. Acta Biotheoretica 44: 95–118.

    Article  PubMed  CAS  Google Scholar 

  • Wichman, H.A., R.A. Van den Bussche, M.J. Hamilton & R.J. Baker, 1992. Transposable elements and the evolution of genome organization in mammals. Genetica 86: 287–293.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, R.K. et al., 1999. How the worm was won. The C. elegans genome sequencing project. Trends Genet. 15: 51–58.

    Article  PubMed  CAS  Google Scholar 

  • Woese, C., 1998. The universal ancestor. Proc. Natl. Acad. Sci. USA 95: 6854–6859.

    Article  PubMed  CAS  Google Scholar 

  • Yang, A.S., M.L. Gonzalgo, J.M. Zingg, R.P. Millar, J.D. Buckley et al., 1996. The rate of CpG mutation in Alu repetitive elements within the p53 tumor suppressor gene in the primate germline. J. Mol. Biol. 258: 240–250.

    Article  PubMed  CAS  Google Scholar 

  • Yoder, J.A., C.P. Walsh & T.H. Bestor, 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13: 335–340.

    Article  PubMed  CAS  Google Scholar 

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Jurka, J., Kapitonov, V.V. Sectorial mutagenesis by transposable elements. Genetica 107, 239–248 (1999). https://doi.org/10.1023/A:1003989620068

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